Affiliations: 1) University of California - Berkeley, Berkeley, CA; 2) Szeged Biological Research Centre, Szeged, Hungary
Keywords: q. adaptation; k. host/pathogen interactions
Symbiotic mutualisms with microbes have played an important role in the evolution of
phenotypic novelties in animals. One of the most striking examples is a protective mutualism
between sap-feeding insects such as the pea aphid (Acyrthosiphon pisum) and the intracellular
bacterial symbiont Ca. Hamiltonella defensa. Some strains of Ca. H. defensa acquired a lysogenic bacteriophage called A. pisum Secondary Endosymbiont (APSE) that encodes diverse bacterial toxins. APSE phages protect insect hosts against parasitoid braconid wasp attack by killing wasp eggs with toxins in the haemocoel. We discovered cytolethal distending toxin B (cdtB) genes encoding CdtB, a widespread DNAse I and virulence factor, were horizontally transferred at least five times from APSE phages to insect nuclear genomes. In Drosophila ananassae, in addition to cdtB, we found two copies of cdtB fused to another apoptosis-inducing toxin gene, apoptosis inducing protein 56 (aip56). We found that expression of these phage-transferred insect cdtB and cdtB::aip56 fusion genes is upregulated in insect fat body and immune cells (hemocytes) after wasp parasitism. Loss-of-function cdtB and cdtB::aip56 mutant lines of D. ananassae were more susceptible to wasp attack than wild-type flies and show phenotypic differences in sexual maturity and development time. Our results show how potent effectors can be co-opted through symbioses to become integral components of animal immune systems.